Diptera, Tabanoidea, Tabanidae) Dorian D

Home , Bromius (beetle), Chrysops caecutiens, Chrysops relictus, Haematopota, Hybomitra, Tabanoidea

Dörge et al. Parasites Vectors (2020) 13:461 https://doi.org/10.1186/s13071-020-04316-7 Parasites & Vectors

RESEARCH Open Access Incompletely observed: niche estimation for six frequent European horsefy species (Diptera, Tabanoidea, Tabanidae) Dorian D. Dörge1*, Sarah Cunze1 and Sven Klimpel1,2

Abstract Background: More than 170 species of tabanids are known in Europe, with many occurring only in limited areas or having become very rare in the last decades. They continue to spread various diseases in animals and are responsible for livestock losses in developing countries. The current monitoring and recording of horsefies is mainly conducted throughout central Europe, with varying degrees of frequency depending on the country. To the detriment of tabanid research, little cooperation exists between western European and Eurasian countries. Methods: For these reasons, we have compiled available sources in order to generate as complete a dataset as possible of six horsefy species common in Europe. We chose Haematopota pluvialis, Chrysops relictus, C. caecutiens, Tabanus bromius, T. bovinus and T. sudeticus as ubiquitous and abundant species within Europe. The aim of this study is to esti- mate the distribution, land cover usage and niches of these species. We used a surface-range envelope (SRE) model in accordance with our hypothesis of an underestimated distribution based on Eurocentric monitoring regimes. Results: Our results show that all six species have a wide range in Eurasia, have a broad climatic niche and can therefore be considered as widespread generalists. Areas with modelled habitat suitability cover the observed distribution and go far beyond these. This supports our assumption that the current state of tabanid monitoring and the recorded distribution signifcantly underestimates the actual distribution. Our results show that the species can withstand extreme weather and climatic conditions and can be found in areas with only a few frost-free months per year. Addi- tionally, our results reveal that species prefer certain land-cover environments and avoid other land-cover types. Conclusions: The SRE model is an efective tool to calculate the distribution of species that are well monitored in some areas but poorly in others. Our results support the hypothesis that the available distribution data underestimate the actual distribution of the surveyed species. Keywords: Tabanidae, Tabanus, Haematopota, Chrysops, Niche, Climate, Land cover, Surface range, Model, Envelope

*Correspondence: [email protected]‑frankfurt.de 1 Institute for Ecology, Evolution and Diversity, Goethe-University, Max‑von‑Laue‑Str. 13, 60439 Frankfurt/Main, Germany Full list of author information is available at the end of the article

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Background bovinus (Linnaeus, 1758) and Tabanus sudeticus (Zeller, Common throughout the world, tabanids are hematopha- 1842). Tabanus spp. and Haematopota spp. are relatively gous dipterans. Worldwide there are about 4400 known eurytopic and do not require stagnant water but moist species [1, 2] of which more than 170 occur in Europe [3]. soil for egg-laying and larval development [25, 39–43], Female horsefies can cause severe skin lesions [4, 5] and while Chrysops belongs to the hydrophilous ecological are able to efectively transmit diferent diseases [6–8] group and depends on ponds, rivers or lakes [44]. due to their excessive feeding behavior [9]. Tese include To fnd a realistic dispersal of the species, we calcu- the eye worm Loa loa (sausing loaiasis) [2, 7, 10, 11], the lated the climatic niche and the land cover allocation of equine infectious anemia virus [12–14], Trypanosoma occurrence points using available literature and database theileri [15, 16] and T. evansi (Surra) which mainly infect data ranging back to 1990. We used the ecological niche livestock [2] but can also infect humans [17]. Further model (ENM) with a surface-range envelope (SRE) to transmittable pathogens are Spiroplasma [18–20], Bacil- project the potential distribution within Europe and Asia. lus tularensis (causing tularemia) [21], Bacillus anthrax In order to counteract the present sampling bias, we used (Anthrax) [12], bovine mycoplasma [22], Elaeophora sch- this method, as it is particularly resistant to over- and neideri (causing elk and deer flariosis) [23] as well as Bes- under-representation of species in databases and litera- noitia besnoiti (causing bovine besnoitiosis) [24]. ture. We also compared the modelled niches (climatic Many species require slow fowing or stagnant water envelopes), as well as the preferred type of land cover and with shallow zones for egg-laying and for the migration of the number of frost-free months required for the six spe- larvae between land and water. Te larvae live predatorily cies to exist. or feed on detritus at the edge of the water, seeking dry ground to pupate. Other species, however, are specialized Methods in drier areas and do not require bodies of water but only For our analysis, we compiled data collected from an moist soil or dung from grazing animals [2, 3, 25–27]. As extensive literature research [37, 45–113] as well as a result of the draining of many of Europe’s wetlands [28, the GBIF-Database [114–120]. Occurrence data were 29], the number of susceptive horsefies has fallen sharply adjusted to the spatial resolution (5 arc-minutes) of the [30]. Current insecticide- and land-use changes are fur- environmental raster data and reduced to one occurrence ther reducing the numbers [31–34]. However, especially per grid cell. in poorer countries, cattle and other livestock continue to sufer due to lack of protection or control options, result- Estimation of the potential distribution ing in anemia or severe skin damage to the afected ani- For the niche range analysis, 8 bioclimatic variables pro- mals [2, 35, 36]. vided by Worldclim [121] were downloaded at a spatial Recent research within Europe is focused mainly on resolution of 5 arc-minutes. Te variables Bio5, Bio6, monitoring points within a few countries for the occur- Bio13, Bio14, Bio18 and Bio19 were used. We computed rence of horsefies and potential control measures [37] SREs (as implemented in the biomod2 R-package [122] as well as ecological and anthropogenic efects on their for each tabanid species and considered three models: populations [38]. To date, there are no standardized and the full model (yellow in the depictions), 95% (orange) repeatedly executed monitoring protocols for horsefies and 90% (red) of all occurrence points. Maps were cre- in Eurasia (and other continents as well), which makes ated in Esri ArcGIS [123]. it difcult to acquire, compile and utilize existing data for calculations and projections. Due to the diferent Comparison of requirements monitoring schemes within diferent countries, occur- Data were acquired from ESA GlobCover [124] for the rences are either over- or underestimated and combin- activity phases, as well as for the land-cover preference ing these datasets is complicated. Based on the lack of comparisons. For the activity comparison, the amount of monitoring in many countries, not much is known about frost-free months was derived from the monthly mini- horsefy complete distribution. Finally, since only sites mum temperature, provided by Worldclim [121]. Te in western Europe have been extensively recorded, the type of land cover was obtained from GlobCover at the distribution in the rest of Eurasia is most likely greatly respective sites for the land-cover comparison and the underestimated. relative frequencies of individual LC-types were com- Six species commonly observed in central Europe were pared with the availability of the LC-type (relative fre- used for our study: Chrysops relictus (Meigen 1820) and quency in the study area). Te range of the study area the morphologically similar species Chrysops caecutiens is reduced to −10°W, 45°E, 79°N and 35°S based on the (Linnaeus, 1758), Haematopota pluvialis (Linnaeus, lack of data from more eastern areas. Land cover cat- 1758), Tabanus bromius (Linnaeus, 1758), Tabanus egories were combined when adequate, resulting in 11 Dörge et al. Parasites Vectors (2020) 13:461 Page 3 of 10

categories: Cropland > 50% (11, 14); Grass/Shrubland with H. pluvialis occurring slightly less frequently and T. (110, 120, 130, 140); Broadleaf Forest (40, 50, 60); Mixed bromius occurring slightly more frequently. Similarly, in Forest (100); Dense Evergreens (70); Light Evergreens Mixed Forest there was only a slightly higher value for T. (90); Mosaic Vegetation (20, 30); Sparse Vegetation (150); bovinus. In the category Dense Evergreens, C. caecutiens, Artifcial (190); Water Bodies (210); and Other (160, 170, C. relictus and T. bovinus showed a negative deviation 180, 195, 215). from the expected value between 60% and 90% while T. bromius (30%) and T. sudeticus (80%) were more com- Results mon. Except for the values, this efect was exactly the Figure 1 shows three diferent models of all six surveyed opposite in the category Light Evergreens. Mosaic veg- species. Te 90% and 95% models for C. caecutiens etation shows no fundamental diference. Sparse Vegeta- showed a very fragmented distribution with the center of tion showed a slight increase in occurrence of T. bovinus, these models lying in the northern part of Europe. Te but a reduction of the other species between 60–180%. full model extended from central Spain over all European Te Artifcial category showed the largest deviations countries, including Turkey and Russia, as far as the east- from the expected value by far, with positive deviations ern part of Siberia. A very similar picture emerged for C. between 260% (2.6 times the expected value) and 510% relictus and H. pluvialis, where only the areas in Spain (5.1 times the expected value). In the Water Bodies cat- and Turkey are missing in the comparison. Incorporat- egory, the values were slightly negative for C. caecutiens, ing the niches’ climatic variables (Fig. 2), all three species C. relictus and T. bovinus, while they are more pro- showed very similar patterns: the 90% and 95% model nounced for the species T. bromius (130%) and T. sudeti- mostly made up less than 50% of the full model and were cus (80%). Te category Other showed medium to strong skewed in one direction. In climatic variable Bio18, C. negative deviations for all species except for T. bovinus. caecutiens showed a higher tolerance for low precipitation than C. relictus and H. pluvialis. Discussion For T. bovinus, T. bromius and T. sudeticus, the 90% and We modelled the potential distribution of six common 95% models were closer to the full model. Te full model horsefy species in Eurasia and compared their niches. closed gaps in central Europe as well as added areas in An SRE model was used because no extensive monitoring (northeastern) Finland and central Russia. For T. sudeti- with standardized methods exists. Hence, the available cus, the full model closed most gaps within the original data show a strong bias with large regions being severely distribution. Te climatic variables (Fig. 2) were relatively underrepresented or not considered at all. Due to the similar for these three species. For T. sudeticus, the 95% very dense sampling in western Europe, a skewed picture model incorporated most of the niche when considering emerges, although several of the species also occur about only the variables. 6000 km further east. Te investigated species require Figure 3 shows that most species (except T. sudeti- moist soil (Tabanus, Haematopota) or lakes, ponds and cus) occur in small numbers in areas with two frost-free rivers (Chrysops) for egg deposition and larval develop- months. Most occurrences are within 9 months for C. ment [25, 39–42]. In addition, the larvae are often detriv- relictus, C. caecutiens and H. pluvialis. Haematopota plu- orous or can feed predatorily on small insects or worms vialis also had a slightly decreased occurrence rate of 11 [125]. Te species are relatively common and widespread months. Te highest numbers of individuals of T. bovinus in Europe and are therefore likely to appear in many sur- occured at 5 and 6 months. Tabanus bromius showed a veys, making them adequate examples for this methodol- steady distribution at 5, 6, 7, 9 and 11 months. Tabanus ogy. For the model, we counteracted the sampling bias as sudeticus showed the most individual occurrences at 7 much as possible by reducing the number of samples to and 11 months. Te data from 5 months on (except for 10 one per grid cell. It is therefore likely that all species can months) showed a slightly lower frequency. No species truly fll most of the niche (full model) calculated in the demonstrated more than 3% of their occurrences in areas analysis. with 10 frost-free months. When comparing the areas of the 90% model, it Te comparison of land cover type and species occur- becomes apparent that the distribution area is very rence (Fig. 4) shows that in the Cropland category, all the small due to a dense monitoring in western and central species occured at a frequency between half and a quar- Europe and a very similar distribution for all six spe- ter of the expected value. Tabanids occured in areas with cies could be expected. When taking the full model into the category Grass/Shrubland between 2–3.5 times the account, a diferent picture emerges. Tree species, i.e. expected frequency, except for T. bovinus, which occured C. caecutiens, C. relictus and H. pluvialis, have a much only slightly more frequently. In Broadleaf Forest, there larger niche than evident from the data. Here, C. cae- were only minor deviations from the expected value, cutiens has the largest distribution and the distribution Dörge et al. Parasites Vectors (2020) 13:461 Page 4 of 10

Fig. 1 Modelled distribution of the six species. Key: yellow, full model; orange, 95% model (5% outliers removed); red, 90% model (10% outliers removed). Figure created with Esri ArcGIS [123] Dörge et al. Parasites Vectors (2020) 13:461 Page 5 of 10

Fig. 2 Comparison of the modelled niches for the six species, Chrysops caecutiens, C. relictus, H. pluvialis, T. bovinus, T. bromius and T. sudeticus, in diferent climatic variables. Abbreviations: Bio5, maximum temperature of warmest month; Bio6, minimum temperature of coldest month; Bio13, precipitation of wettest month; Bio14, precipitation of driest month: Bio18, precipitation of warmest quarter; Bio19, precipitation of coldest quarter. Key: yellow, full model; orange, 95% quantile model; red, 90% quantile model

Fig. 3 Percentage occurrence as a function of the number of frost-free months. For each species, the sum of all categories equals 100%. Abbreviation: mo, months areas of the other three species overlap even in the by data collection in Europe. Tabanus sudeticus has eastern areas, where only few surveys have been made. the smallest distribution. Te distribution of collected Tabanus bovinus and T. bromius have similarly large sightings of T. bovinus and the results of our calculation niches which are mostly overlapping and are supported Dörge et al. Parasites Vectors (2020) 13:461 Page 6 of 10

Fig. 4 Deviation of occurrence of the species compared to available land cover. A positive value of 100% shows that the species occurs twice as often as expected in the respective areas. Conversely, a negative value of 100% indicates an abundance that is only half as high as expected

are very close to the known distribution which is shown surprising that grassland and scrubland are preferred. in Fig. 1. Since Grasslands, or areas with some lowland scrub, are mostly used as grazing land for livestock [130], tabanids can easily fnd the hosts they need. Broadleaf forest, Activity phases mixed forest and mosaic vegetation show no particular When comparing the frequency of occurrence as a efect on tabanid preference or aversion. However, Dense function of the number of frost-free months, it is Evergreen and Light Evergreen showed an interesting pat- apparent that fve of the six species can occur in areas tern on preference and aversion, which largely balances with only two frost-free months, albeit with only a few out when the two categories are combined. We remark individuals. Tis frequency gradually increases up to that C. relictus, C. caecutiens and T. bovinus avoid dense fve months, with T. sudeticus appearing in areas with evergreen, while at least T. sudeticus prefers it. Sparse at least four frost-free months. Te remaining numbers vegetation is avoided by all species except for T. bovinus. show the direct infuence of the sampling bias towards Tis can be explained by the fact that within these areas, central and western Europe. Te extreme peak at nine signifcantly fewer animals can serve as hosts. An inter- months is mainly due to heavy sampling in central esting result is that all species have an extreme prefer- Europe, while the increased numbers at 11 months are ence for Artifcial areas category. Tis is most likely due almost entirely due to the inclusion of England and Ire- to the fact that populated areas harbor domestic animals, land. It is known that horsefies hibernate as larvae and grazing animals, livestock and, ultimately, people in the may require several years for their development [126]. immediate vicinity. It is important to note that although In central Europe, development spans between one and the dataset has been adjusted and reduced to one point three years. However, assuming an area with only two per grid cell, a sampling bias is still present towards heav- frost-free months per year, this number could increase ily populated as well as frequently surveyed areas. Tis signifcantly. Te most cold-tolerant species are C. cae- would explain at least part of the extreme values of the cutiens, C. relictus and H. pluvialis with occurrences in Artifcial category. Baldacchino et al. [38] were able to areas that plunge below −58 °C. show parts of the current horsefy diversity of western and southern European countries in a large-scale study of Land‑cover comparison almost 80,000 captured animals. In comparison to other As expected, monoculture cropland was avoided by all areas, a signifcantly lower diversity of species could be six species. Tis may be due to pesticide use, lack of hosts found on pastureland, with larger, well-fying species pre- and lack of areas for egg-laying and larval development ferring these areas for host searching. Another study by and lack of adequate sites for mating behavior, as well Baldacchino et al. [113] also suggested a preference for as a shortage of sugar sources [127–129]. It is also not mosaic landscape and light forest. Our analysis cannot Dörge et al. Parasites Vectors (2020) 13:461 Page 7 of 10

confrm this result since our dataset does not support any Conclusions preference for mosaic landscape. On the other hand, our Te distribution of most tabanids is not monitored analyses show that forest cover presents mixed results enough in many areas. Te SRE model is an efec- for aversion or preference by the examined species. Te tive tool to calculate the distribution of species that are land-cover analysis also shows that tabanids equally well monitored in some areas but poorly in others. Our colonize water bodies if they are available. However, the results support the hypothesis that the available distri- numbers mostly show an underrepresentation, which is bution data underestimate the actual distribution of the explained by the fact that the available land cover is taken surveyed species. Especially C. relictus, C. caecutiens and with a resolution of 300 meters, so most water bodies H. pluvialis have a much larger calculated niche than the are not presented in the dataset. Te category “Other” collated observations represent. Our results also show consists of several land-cover types with very few occur- that fve of the six species occur in areas with only two rences and should therefore, be considered carefully if at frost-free months per year, revealing a strong resistance all. Overall, we have reduced the infuence of sampling against temperatures up to −58 °C. We found that the biases as much as possible, but the efects still shift our six species of horsefies strongly prefer populated areas, results. A standardized monitoring programme is needed as well as grassland and scrubland and avoid arable land to clarify these results and enable future calculations to and regions of sparse vegetation. Our results reveal be more exact. that only the observed distribution of T. bovinus closely resembles the calculated niche while the other species are Quality of the model most likely not monitored enough. Both Chrysops spe- Our envelope model included Japan as a suitable area for cies have almost the same observed distribution and cal- all species. Tis is highly unlikely, at least for the three culated niche, as well as land-cover preferences. We also Tabanus species. According to the GBIF database, H. plu- suggest a standardized monitoring programme, which vialis occurs in Japan. However, this isolated occurrence can improve and validate this methodology for tabanids was not included in the calculation due to the extreme and other species. With the help of predictions from this distance to other sites but is a realistic occurrence point model, further monitoring can be planned in areas where for this species after calculating the model. Other remote few or no observations have been recorded to confrm areas such as the Asian Highlands (Pamir, Hindukush, and extend our model. Himalaya) were additionally estimated as suitable sites Acknowledgements by our model. We doubt that these mountain ranges are We thank Dr. Adrienne Jochum for proofreading the manuscript. actually suitable areas for tabanid habitation and that an Authors’ contributions exclusionary factor is lacking in the model. For the three DDD designed and conceptualized the study, wrote the main manuscript text, Tabanus species specifcally, it is very unlikely that they executed the statistical analysis, interpreted the data and prepared Figs. 2, 3, can be found in these areas. For Chrysops species and H. 4. SC executed the statistical analysis, interpreted the data and prepared Fig. 1. SK designed and conceptualized the study. All authors read and approved the pluvialis, however, the areas are within the range of the fnal manuscript. main distribution spectrum but are discontinuous. We considered temperature and precipitation as important Funding Open access funding provided by Projekt DEAL. This research was funded climatic factors. Tere can also be other factors that are by the German Federal Ministry of Food and Agriculture (BMEL) through the not considered in this study, but which locally exclude Federal Ofce for Agriculture and Food (BLE) (Grant Numbers 2819104415 and the occurrence of these species (e.g. snow cover, humid- 2819105115) and by the Uniscientia Foundation (P 121-2017). ity). Our model is based on a continental scale, where Availability of data and materials climatic factors are the most important to show rough The data are available through the cited references as stated in the Methods distribution patterns [131]. Fine-scale models could go section. into more detail and include microclimatic efects, but Ethics approval and consent to participate due to the continental scale and the lack of available data, Not applicable. this is beyond the scope of this study. Te delimited parts Consent for publication of the model (e.g. southern China, mountain ranges of Not applicable. Asia) in which some species could occur due to a calculated suitable habitat, but either do not occur or it is Competing interests unknown, show possible distribution areas, which, how- The authors declare that they have no competing interests. ever, have not been colonized due to dispersal barriers or Author details a missing limiting factor. 1 Institute for Ecology, Evolution and Diversity, Goethe-University, Max‑von‑Laue‑Str. 13, 60439 Frankfurt/Main, Germany. 2 Senckenberg Biodi- versity and Climate Research Centre, Senckenberg Gesellschaft für Natur- forschung, Senckenberganlage 25, 60325 Frankfurt/Main, Germany. Dörge et al. Parasites Vectors (2020) 13:461 Page 8 of 10

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